Pollen morphology and taxonomy of Atraphaxis (Polygoneae, Polygonaceae) O. V. Yurtseva, E. E. Severova & I. Yu. Bovina Plant Systematics and Evolution ISSN 0378-2697 Volume 300 Number 4 Plant Syst Evol (2014) 300:749-766 DOI 10.1007/s00606-013-0917-4 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag Wien. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Plant Syst Evol (2014) 300:749–766 DOI 10.1007/s00606-013-0917-4 ORIGINAL ARTICLE Pollen morphology and taxonomy of Atraphaxis (Polygoneae, Polygonaceae) O. V. Yurtseva • E. E. Severova • I. Yu. Bovina Received: 21 June 2013 / Accepted: 7 September 2013 / Published online: 15 October 2013 Ó Springer-Verlag Wien 2013 Abstract Pollen grains of 32 species of Atraphaxis L. characters and probable interspecific hybridization. The including six species previously attributed to Polygonum L. genus Atraphaxis L. comprises about 30 species distributed s.str. were investigated with LM (acetolysed pollen) and throughout Southeastern Europe, Southwestern and Central SEM (dry pollen). Pollen grains of all studied species are Asia, South Siberia, Mongolia, and China (Pavlov 1936; spheroidal to oblong-spheroidal, mostly tricolporate, rarely Borodina 1989; Lovelius 1979). 4-6-loxocolporate, ellipsoidal in equatorial view, rounded- Based on the presence of shrubby life form and woody trilobed or trilobed in polar view, with striate or striato- pith parenchyma, Dammer (1893) attributed Atraphaxis, perforate, reticulato-foveolate, or reticulato-perforate Pteropyrum Jaub. et Spach and Calligonum L. to the tribe sporoderm ornamentation. Exine sculpture is the most Atraphaxideae, while Perdrigeat (1900) moved them to the variable feature, differing in width, distinctness, and tribe Calligoneae, and Gross (1913)—to subtribe Atraph- spacing of the striae, which are divided by grooves with axinae of the tribe Polygoneae. Haraldson (1978) specu- small pits or perforations in rows. The most distinct vari- lated that Atraphaxis was an ancestor of Polygonum L. ants of sporoderm ornamentation are connected by a full s.str., on the basis of both sharing lignificated collenchyma, range of transitions. Striato-perforate ornamentation is assimilation tissue and absciss layer in the petiole, assim- common in species with the perianth typical for ilation tissue in the stem and both lacking trichomes on the Atraphaxis, whereas reticulato-foveolate or reticulato-per- filaments. Atraphaxis and Polygonum L. s.str. possess forate sporoderm ornamentation was found in species with thyrses with axillary cymes of flowers (Gross 1913). the perianth of Polygonum-type. Similarity of Atraphaxis, Polygonum L. s.str. and Polygo- nella Michx. was demonstrated in petiole and stem anat- Keywords Atraphaxis Á Polygonum Á Polygonaceae Á omy, and in the structure of perianth and fruit (Haraldson Pollen Á Sporoderm Á Taxonomy 1978; Ronse Decraene and Akeroyd 1988; Ronse Decraene et al. 2000). The genus Polygonum L. s.str. has the cam- panulate perianth with a short and wide tube and oblong Introduction tepals of equal size, the genus Atraphaxis differing by the perianth with a long filiform tube and 4–5 tepals, the inner The taxonomy of the genus Atraphaxis L. is complex ones becoming significantly enlarged in fruiting (Linnaeus and uncertain due to high variability of morphological 1753; Boissier 1879; Brandbyge 1993). Recent molecular-phylogenetic reconstructions based on chloroplast genes (rbcL, matK, trnL, trnF), nuclear gene O. V. Yurtseva (&) Á E. E. Severova Á I. Yu. Bovina LEAFY and ITS 1–2 sequences confirmed that Atraphaxis Department of Higher Plants, Faculty of Biology, is closely related to Polygonum L. s.str. and Polygonella Lomonosov Moscow State University, Leninskie Gory, 1-12, 119 991 Moscow, Russia Michx., all three attributed to the tribe Polygoneae along e-mail: [email protected] with Knorringia (Chukav.) Tzvelev, Fallopia Adans., E. E. Severova Muehlenbeckia Meisner, Reynoutria Houtt., and Duma e-mail: [email protected] T.M.Schust., whereas Calligonum and Pteropyrum belong 123 Author's personal copy 750 O. V. Yurtseva et al. to the tribe Calligoneae (Lamb Frye and Kron 2003; San- blades served as a basis for recognition of three sections chez et al. 2009, 2011; Schuster et al. 2011a, b). The (Aleshina et al. 1978; Lovelius and Sjabrjaj 1981). Section affinity of Atraphaxis and Polygonum was confirmed by the Atraphaxis L. (A. spinosa, A. replicata, A. karataviensis, analysis of chloroplast regions (Tavakkoli et al. 2010; Sun A.compacta) with dimeric flowers and short lateral thyrses and Zhang 2012). is characterized by spheroidal slightly trilobed pollen with Our phylogenetic investigations of the tribe Polygoneae small endoapertures and distinct columellae with closed based on nuclear ITS 1–2 sequences showed the affinity capita. Section Tragopyrum (Bieb.) Meissn. (A. musch- of Atraphaxis to Fallopia, Polygonella, and Polygonum ketowi, A. caucasica, A. pyrifolia, A. laetevirens, A. bil- (Yurtseva et al. 2010, 2012a, b, c). In ML-tree three species lardierei, A. avenia, A. frutescens, and A. badhysi) with of Polygonum (Polygonum arianum Grigorj., P. atraphax- pentamerous perianth, trimeric gynoecium, and long lateral iforme Botsch., and P. toktogulicum Lazkov) entered the and terminal thyrses differs by distinctly trilobed pollen clade of Atraphaxis. Schuster et al. (2011b) transferred grains with elliptic endoapertures and thin columellae with them to the genus Atraphaxis with new nomenclature slightly closed capita. Atraphaxis teretifolia (Popov) combinations. Our recent analysis based on the extended Komarov ex Pavlov (=Atraphaxis jrtyschensis Chang data on ITS 1–2 fragments (Yurtseva et al. in preparation) Y.Yang & Y.L.Han) from monotypic section Physopyrum showed that in ML-tree Atraphaxis atraphaxiformis (Popov) Lovelius differs by lineate leaves and has small (Botsch.) T.M.Schust. & Reveal (=Polygonum atraphaxi- oblong slightly trilobed pollen grains with distinct endo- forme Botsch.), Atraphaxis toktogulica (Lazkov) apertures and thin columellae with non closed capita. Bo- T.M.Schust. & Reveal (=Polygonum toktogulicum Lazkov), vina (1996) studied sporoderm sculpture (SEM) of 21 Atraphaxis tortuosa Losinsk. (=Polygonum tortuosum species of Atraphaxis from the territory of the former (Losinsk.) Lovelius), and Atraphaxis ariana (Grigorj.) USSR and described four types of sporoderm ornamenta- T.M.Schust. & Reveal (=Polygonum arianum Grigorj.) are tion, which do not consistent with sections or subgenera nested among typical members of Atraphaxis, while within the genus. P. ovczinnikovii Chukav. occupies basal position in the Bao and Li (1993) studied sporoderm of pollen grains clade of Atraphaxis. Hereafter these species will be treated (SEM) in ten species of Atraphaxis from China and dis- as the members of the genus Atraphaxis. These taxa as well tinguished two types of the sporoderm ornamentation: as P. popovii Borodina are characterized by campanulate striate (A. pungens, A. jrtyschensis, A. laetevirens, A. deci- perianth typical for the genus Polygonum; therefore, they piens, A. pyrifolia) and striato-reticulate (A. frutescens, were initially or later classified as the members of the genus A. spinosa, A. compacta, A. bracteata, A. manshurica), Polygonum (Grigorjev 1933; Komarov 1936; Chukavina which do not correspond to the taxonomic division of the 1962, 1968, 1971; Botschantzev 1965; Lovelius 1975; genus Atraphaxis. Ge and Liu (1994) studied pollen grains Borodina 1989; Lazkov and Sultanova 2002). in 12 species of Atraphaxis from China. In most of The genus Atraphaxis L. was formed by combining the the studied species the pollen grains were prolate or sub- genera Tragopyron Bieb. and Atraphaxis L. by Jaubert and prolate with striate sporoderm ornamentation (A. replicata, Spach (1844–1846) who subdivided Atraphaxis into sub- A. spinosa, A. compacta, A. laetevirens, A. virgata, genera Euatraphaxis, Tragatraphaxis, and Tragopyrum. A. frutescens, A. decipiens, A. jrtyschensis, A. pungens, Later, taxonomists recognized two to five sections or sub- A. muschketowi, A. pyrifolia), with an exception of genera in the genus Atraphaxis based on flower merosity and A. bracteata that differs from other species by more inflorescence structure (Meisner 1857; Boissier 1879;Kras- elongated pollen (P:E = 1.88) with striato-reticulate nov 1888; Pavlov 1936; Aleshina et al. 1978; Lovelius 1979). ornamentation. Zhou et al. (1999) characterized pollen The data on pollen grains of Atraphaxis are incomplete surface of A. manshurica and A. laetevirens as striato- and often controversial. Pollen grains were described for perforate. some species as 3-(4)-colporate, spheroidal-prolate or Borzova and Sladkov (1969) showed that pollen of prolate, rounded or elliptical in equatorial view, round- Polygonum ovczinnikovii (=Atraphaxis ovczinnikovii) and trilobed in polar view, with